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The Aetiology and Pathogenesis of Tropical Ulcer

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The Aetiology and Pathogenesis of Tropical Ulcer The Aetiology and Pathogenesis of Tropical Ulcer Town Beverley Adriaans Tropical DermatologyCape Unit Department ofof Medical Microbiology London School of Hygiene and Tropical Medicine Keppel Str eet London WClE 7HT England University A Thesis presented for the M.D. degree in the University of Cape Town, South Africa, 1988 . The copyright of this thesis vests in the author. No quotation from it or information derived from it is to be published without full acknowledgementTown of the source. The thesis is to be used for private study or non- commercial research purposes only. Cape Published by the University ofof Cape Town (UCT) in terms of the non-exclusive license granted to UCT by the author. University ABSTRACT Tropical ulcer is a very specific form of cutaneous ulceration. It occurs worldwide in most tropical and a number of subtropical areas. The disease occurs mainly in older children and young adults with children under the age of 5 and adults over 45 years rarely being affected. Ulcers occur most commonly on the lower leg but may occur on the upper limb. Although most ulcers normally heal slowly over many weeks or months, some ulcers may recur. Recognised complications include squamous cell carcinoma, gangrene and osteitis, although these are rare. A number of authors have reported on the disease and suggested diet, trauma and infection as aetiological factors for this condition. This survey was thus conducted to assess as many of these factors as possible. The study took place in 5 tropical areas, namely Zambia, Gambia, southern India, Fiji and Papua New Guinea. Consultations took place at hospitals, rural clinics, health centres and villages. Although many authors have suggested that the disease is related to malnutrition, few have objectively assessed the nutritional status of the patients and compared it with controls. Those studies which included objective assessments were limited to small areas and only investigated specific parameters. In order to investigate the immune response of the host to an anaerobic infection, the antibody levels to the organisms isolated from the ulcers were measured by an ELISA test . The local host response to an infection with a Fusobacterium species was assessed by the number of antibody secreting B-lymphocytes at the site of the ulcers. These parameters ma y play a role in the localisation of the ulcers and account for recurrent infections . In this survey the nutritional status of the patients was objectively assessed and compared to a control population in each area. A questionnaire was used to obtain personal details and information about the present and/ or previous ulcers . Several authors have also reported fusiform bacilli and spirochaetes on smears from the ulcers. These organisms have not been fully characterized as they are anaerobic bacteria and require a strict anaerobic environment to survive . A suitable transport sys tem wa s therefore developed to transport the specimens from the tropical study areas to London. This kept the samples anaerobic and ensured that the organisms remained viable. During this study, swabs were taken from the base of the ulcers and biopsies from the edge. Both types of samples were examined bacteriologically and all were cultured aerobically and anaerobically . The biopsies were also examined histologically . Electron microscopy was performed on some biopsies. Th e isolates were tested for in-vitro cytotoxicity as a possible mechanism for the development of ulcers . The pathogenicity of all the bacterial species recovered from the ulcers was further assessed by their ability either singly, or in combination, to induce an experimental abscess in a guinea pig . In-vivo synergy between the various organisms was also investigated. The guinea pig proved to be the most suitable animal model . Acknowledgements I would like to thank my two supervisors at the London School of Hygiene and Tropical Medicine, Dr Roderick J Hay, Reader in Clinical Mycology and Dr Bohumil S Drasar, Reader in Bacteriology for their help, encouragement and constant advice in conducting this research and Zerin Ahmet, for the technical help she provided throughout the research. Dr Derek Robinson very kindly collected samples and data from some of the areas surveyed. My research was generously supported by the Wellcome Trust. CONT ENT S Page SUMMARY l INTRODUCTION Study plan 3 REVIEW OF THE LITERATURE 7 Epidemiology 8 Clinical manifestations 16 Nutritional status 25 Role of infection 32 Pathology 41 Management 43 CURRENT STATE OF THE PROBLEM 48 MATERIALS AND METHODS Epidemiology 50 Clinical manifestations 53 Nutritional status 59 Role of infection 61 Pathology 90 Mechanisms of infection 102 RESULTS Epidemiology 116 Clinical manifestations 121 Nutritional status 136 Role of infection 145 Pathology 172 Mechanisms of infection 191 DISCUSSION 208 CONCLUSION 218 APPENDIX l Tropical ulcer questionnaire 220 Transport fluid 226 Medium for spirochaete isolation 227 Ingredients for PAGE 228 Cell growth medium 229 APPENDIX 2 Suppliers 230 BIBLIOGRAPHY 235 LIST OF FIGURES Fig. 1. Distribution of tropical ulcer. Fig. 2. Schematic representation of ulcer progression. Fig. 3. Parts of a Hungate tube. Fig. 4. Cannulae for delivery of gas. Fig. 5. Method for preparation of transport fluid. Fig. 6. Hungate tube with anaerobic transport fluid. Fig. 7. Hungate tube showing loss of anaerobiasis. Fig. 8. Acute tropical ulcer. Fig. 9. Chronic ulcer. Fig. 10. Multiple tropical ulcers well separated. Fig. 11. Multiple adjacent tropical ulcers . Fig. 12. Squamous cell carcinoma . Fig. 13. Histology of squamous cell carcinoma. Fig. 14. Tropical ulcer scar. Fig. 15. Tropical ulcer and early leishmaniasis. Fig. 16. Histology of leishmaniasis. Fig. 17. Leishmaniasis in a child. Fig. 18. Fusobacterium type l colony. Fig. 19. Fusobacterium tupe l morphology. Fig. 20. Fusobacterium type 2 colony. Fig. 21. Fusobacterium type 2 morphology. Fig. 22. Electron microscopy of Fusobacterium type 1. (BHI ) Fig. 23. Electron microscopy of Fusobacterium type l. (FABA ) Fig. 24. Electron microscopy of Fusobacterium type 1. (WC ) Fig. 25. Electron microscopy of Fusobacterium type 2. ( BHI ) Fig. 26 PAGE of Fusobacterium types land 2. Fig. 27. PAGE of Fusobacterium types land 2, and other species of Fusobacterium. Fig. 28. Carbal fuchsin stain of cultured spirochaetes. Fig. 29. Histology of tropical ulcer showing spongiosis. Fig. 30. Histology showing vascular changes. Fig. 31. Dieterle stain showing bacteria. Fig. 32. Dieterle stain showing spirochaetes. Fig. 33. Electron microscopy of fusobacteria in the dermis Fig. 34. Electron microscopy of spirochaete in the dermis Fig. 35. Immunohistochemistry ( T-cells ) of infiltrate. Fig. 36. Immunohistochemistry (B-cells ) of infiltrate. Fig. 37. Vero cells in culture with medium. Fig. 38. Vero cells exposed to Fusobacterium supernatant. Fig. 39. Mouse model showing cutaneous necrosis. Fig. 40. Guinea pig model showing abscess formation. Fig. 41. Histology of experimental ulcer. LIST OF TABLES 1. Nutrition and tropical ulcer. 2. The role of infection in tropical ulcer. 3. Bacterial culture media. 4. Selective media for bacterial culture. 5. In-vitro cytotoxicity cell lines. 6. Bacterial strains for in-vitro cytotoxicity. 7. Bacterial strains for animal inoculations. 8. Mouse strains for animal inoculations. 9. Frequency of tropical ulcer in Papua New Guinea. 10. Number of tropical ulcers per location. 11. Number of ulcers per patient. 12. Anatomical sites of tropical ulcers. 13. Age distribution of patients with tropical ulcers. 14. Sex of patients with tropical ulcers. 15. Relationship of tropical ulcers and trauma. 16. Body mass index of patients with tropical ulcers. 17. Body mass index of ulcer patients and controls. 18. Dermatophyte infections in Fiji. 19. Number of swabs analysed per location. 20. Bacterial isolates from each location. 21. Number of isolates per swab. 22. Analysis of single isolates. 23. Frequency of multiple anaerobic isolates. 24. Bacterial species recovered from swabs. 25. Duration of ulcer and recovery of anaerobes. 26. Number of isolates from mud samples. 27. Biochemical profile of fusobacteria isolated. 28. Different characteristics of Fusobacterium species. 29. Characteristics of Bacteroides species isolated. 30. Pathology of tropical ulcer. 31. Patient serology - antibody levels to fusobacteria. 32. ELISA - antibody to bacteria from the ulcers. 33. ELISA - Rabbit IgG levels. 34. ELISA - Rabbit IgM levels. 35. Percentage of Vero cells affected. 36. Cell lines and cytotoxicity. 37. Cytotoxicity of supernatant fractions. 38. Butyrate concentrations causing cytotoxicity. 39. Inoculation of single bacteria. 40. Inoculation of multiple organisms. SUtf1ARY Tropical ulcer is an acute or chronic skin disease seen in the tropics and subtropics that is characterized by necrosis of the epidermis and underlying subcutaneous tissue. The disease has been reported from China to the West Indies . Although it occurs mainly in children adults may also be affected. The disease often ha s a protracted course as the ulcers may continue for several months . Previous reports on the disease, over the past 90 years, have included diet, trauma and infection as aetiological agents. This study investigated one hundred and seventy-nine patients with tropical ulcers in five tropical areas. The nutritional status of the patients was assessed objectively . This study shows that there was no consistent relationship to overt malnutrition. The clinical, bacteriological and histological
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